Host-Parasite Cospeciation

Key Questions

• Is the parasite an heirloom or a souvenier?

• Is the association ancient or recent?

• What processes are involved?

• Is there coevolution?

• Is there correlated evolution?

Coevolution: coadaptation and cospeciation

• Coadaptation = reciprocal adaptation

• Cospeciation = joint speciation of host and parasite

Farenholz’s Rule

• Farenholz’s rule - parasite phylogeny mirrors host phylogeny

• Implies we can use parasite phylogeny to infer host phylogeny

Modern Cospeciation Studies

• Construct host and parasite phylogenies independently.

• Test for cospeciation (don’t assume it).

• Use molecular phylogenies so we can compare rates of evolution.

Host Parasiteincongruence

congruence(cospeciation)

(not cospeciation, e.g. host switching)

Incongruence signals processes other than cospeciation

independent speciationhost switchcospeciation

"missing the boat"extinction

host

parasite

(a) (b)

(e)(d)

(c)

failure to speciate

(f)

Testing hypotheses of cospeciation

• Would we get host and parasite phylogenies that are this similar due to chance alone?

• Can test using random trees: generate many (>100) random parasite trees and see how similar they are to the host tree.

Same topologies, speciation times, and rates of evolution

Same topologies and times of speciation

Same tree topologies(a)

(b)

(c)

Lice as a “model system”

• Methods for comparing host and parasite phylogenies

• Comparative molecular evolution

• Factors involved in cospeciation

• Factors involved in host specificity

GenusFamilySuborder

Anoplura532

Ischnocera3,060

1,344Amblycera

birdmammal

Kim, 1988

Paterson et al,2000

Smith, 2000

Smith, 2000

Barker, 1991

Clayton et al, 1996

Page et al, 1995Hafner et al, 1994

Lyal, 1985a

Rhyncophthirina2

Clay, 1969

Host:

Why lice are nice...

• Obligatory, permanent parasites

• Single host during life cycle

• Ectoparasites (easy to manipulate)

• High degree of cospeciation

Why lice are lousy...

• Single origin of parasitism

• No endoparasitic lice

• Single host during life cycle

• Not (very) virulent

• c.f. mites

Gophers and LiceO. hispidus

T. bottae

T. talpoides

G. personatus

G. breviceps

G. bursarius (a)

G. bursarius (b)

C. merriami

P. bulleri

O. cavator

O. cherriei

O. underwoodi

C. castanops

O. heterodus

Z. trichopus

G. chapini

G. setzeri

G. thomomyus

G. perotensis

T. minor

T. barbarae

G. trichopi

G. nadleri

G. expansus

G. geomydis

G. oklahomensis

G. ewingi

G. texanus

G. actuosi

G. panamensis

G. cherriei

G. costaricensis

Swiftlets and Dennyus liceChaetura pelagica

Chaetura vauxi

C. esculenta nitens

C. esculenta bagobo

C. esculenta marginata

C. esculenta cyanoptila 1

C. esculenta cyanoptila 2

C. linchi

A. elaphrus

A. francicus

A. spodiopygius assimilis 1

A. mearnsi

A. vanikorensis palawanensis

A. fuciphagus vestitus

A. salanganus natunae

A. spodiopygius assimilis 2

A. s. spodiopygius

A. maximus lowi

A. brevirostris vulcanorum

A. terraereginae

Cypsiurus balasiensis

Cypsiurus parvus

D. dubius

D. vauxi

Dennyus sp. 1

D. distinctus ssp.

D. distinctus timjonesi

D. d. distinctusD. somadikartai 1

D. somadikartai 2

D. carljonesi fosteri

D. carljonesi forresteri

D. hahnae

D. c. carljonesi

D. singhi

D. kristinae

D. wraggi

D. simberloffi

Dennyus sp. 2D. wellsi

D. thompsoni

D. collinsi

D. adamsae

D. cypsiurus 1

D. cypsiurus 2

Song birds and Brueelia liceAratinga astecNyctibius jamaicensisFormicarius moniligerThamnophilus doliatusPloceus velatusCacicus haemorrhousCarpodacus mexicanusPycnonotus nigricansHypsipetes philippenisParisoma subcaeruleum

Parus nigerParus elegansSitta frontalisFicedula hyperythraRhipidura nigrocinnamomeaCoracina striata

Cyanocorax morioTrogon massenaTrogon melanocephalusMomotus momotaMelanerpes candidusAndigena nigrirostrisAulacorhynchus prasinusMegalaima monticolaMegalaim mystacophanos

Nyctibicola longirostris

Paragoniocotes sp.

Formicaricola analoides

Formicaphagus sp.

Brueelia sp. 7

Brueelia sp. 6

Brueelia sp. 8

Brueelia sp. 11

Brueelia sp. 9

Brueelia sp. 10

Brueelia sp. 12

Brueelia sp. 5

Brueelia moriona

Brueelia sp. 2

Brueelia sp. 1

Brueelia sp. 3

Brueelia laticeps

Brueelia marginella

Brueelia sp. 4

Correlated evolution

• Relative rates of molecular evolution

• Host and louse body size

• Host and parasite speciation rates

Relative rates of molecular evolution

• Molecular data is comparable between hosts and parasites (unlike morphological data)

• Can use homologous genes to compare rate of evolution (e.g., cytochrome oxidase I in birds and lice)

• Louse mitochondrial genes evolve 2-3 times more rapidly than bird and mammal genes

220

240

260

280

300

320

340

3.00 3.50 4.00 4.50 5.00 5.50 6.00 6.50

Lou

se m

etat

hora

cic

wid

th (

µm

)

ln (Host body mass in grams)

Big birds have big lice

Head groove width correlates with hair width

40 50 60 70 8030

40

50

60

70

80

Gro

ov

e D

iam

ete

r o

f C

he

win

g L

ou

se

(µm

)

Hair Diameter of Pocket Gopher (µm)

host clade

first parasite clade

second parasite clade

Time

2T

1T

Replicate lineages

• Multiple parasites on the same host• Can test hypotheses concerning patterns and

processes

Phoebetria palpebrata

Diomedea chrysostoma

Diomedea bulleri

Diomedea epomophora

Diomedea exulans

Diomedea irrorata

Diomedea nigripes

Diomedea immutabilis0.1

79 Paraclisis diomedeae

78 Paraclisis diomedeae

77 Paraclisis diomedeae

81 Paraclisis hyalina

82 Paraclisis hyalina

80 Paraclisis giganticola

83 Paraclisis miriceps

76 Paraclisis confidens

Diomedea bulleri

Diomedea exulans

Diomedea epomophora

Diomedea immutabilis

Diomedea irrorata0.1

291 Docophoroides harrisoni

290 Docophoroides brevis

289 Docophoroides brevis

293 Docophoroides niethammeri

292 Docophoroides levequei

Distribution of two louse genera

How do multispecies How do multispecies assemblages arise?assemblages arise?

Host species A Host species B

“head” lice

“wing” lice

GenusFamilySuborder

Anoplura532

Ischnocera3,060

1,344Amblycera

birdmammal

Kim, 1988

Paterson et al,2000

Smith, 2000

Smith, 2000

Barker, 1991

Clayton et al, 1996

Page et al, 1995Hafner et al, 1994

Lyal, 1985a

Rhyncophthirina2

Clay, 1969

Host:

How old are lice w.r.t. How old are lice w.r.t. their hosts?their hosts?

present day

time

lice younger lice same age lice older

radiation of modern birds radiation of

bird lice

Microraptor gui, an early Cretaceous feathered dinosaur

Fossil bird louse from Eocene (44 Mya)

Summary

• Host-parasite cospeciation is an instance of a more general problem (“historical associations”).

• We can use phylogenies for host and parasite to test hypotheses of cospeciation.

• Lice are an excellent group for cospeciation studies.